Cleaner fish cause predators to reduce aggression toward bystanders at cleaning stations

Mutualisms, in which both participants gain a net benefit, are ubiquitous in all ecosystems, and the importance of understanding their broader ecological context has been demonstrated many times. Indirect effects of mutualisms may have important implications for surrounding ecosystems through changes in density, species composition, or behavior; however, the latter has been difficult to quantify. In fish cleaning mutualisms, cleaners benefit by removing and consuming ectoparasites from clients, whereas clients benefit from a reduction in parasite load. Cleaner fish are also thought to benefit from immunity to predation and use tactile stimulation as a preconflict management strategy to manipulate partners' decisions and to avoid being eaten by piscivorous client fish. Here we show, using a laboratory experiment, that the presence of cleaner fish resulted in nearby fish not involved in the cleaner-client mutualism experiencing less aggression (chases) from predatory clients. In addition, the rate that piscivorous clients chased prey was negatively correlated with the amount of tactile stimulation given to the predator by the cleaner. These data suggest that, in the laboratory, the risk of aggression from predators toward nearby prey fish was greatly reduced as a by-product of cleaner fish presence and tactile stimulation of predators by cleaner fish. These results raise the question of whether cleaning stations act as safe havens from predator aggressio

Tropical range extension for the temperate, endemic South-Eastern Australian Nudibranch Goniobranchus splendidus (Angas, 1864)

In contrast to many tropical animals expanding southwards on the Australian coast concomitant with climate change, here we report a temperate endemic newly found in the tropics. Chromodorid nudibranchs are bright, colourful animals that rarely go unnoticed by divers and underwater photographers. The discovery of a new population, with divergent colouration is therefore significant. DNA sequencing confirms that despite departures from the known phenotypic variation, the specimen represents northern Goniobranchus splendidus and not an unknown close relative. Goniobranchus tinctorius represents the sister taxa to G. splendidus. With regard to secondary defences, the oxygenated terpenes found previously in this specimen are partially unique but also overlap with other G. splendidus from southern Queensland (QLD) and New South Wales (NSW). The tropical specimen from Mackay contains extracapsular yolk like other G. splendidus. This previously unknown tropical population may contribute selectively advantageous genes to cold-water species threatened by climate change. Competitive exclusion may explain why G. splendidus does not strongly overlap with its widespread sister taxon

Regulation, constraints and benefits of colour plasticity in a mimicry system

Rapid colour change is used in aggressive interactions, ontogenetic transitions, nuptial displays and to prevent detection and/or recognition from predators or prey. The underlying mechanisms, constraints and benefits of colour change are often unclear, but examining such factors offers insights into phenotypic plasticity. Here, we investigated the mechanisms behind how an aggressive reef fish mimic (bluestriped fangblenny Plagiotremus rhinorhynchos) changes colour rapidly (1-5 min) between mimetic and other colour forms. Black with one neon blue dorsal stripe (mimic), black with two neon blue stripes, brown, olive and orange forms differed in melanophore density. Fish skin biopsies were modulated in vitro by hormones, and smaller fangblennies changed coloration more rapidly than larger fish suggesting that the ability to change colour is diminished as fish get larger. Individuals may be limited by differences in pigment cell densities to change colour between extreme colour forms (black to orange); therefore, longer morphological changes may also occur or fangblennies may exhibit dimorphic populations. Behavioural observations suggest that small black and orange individuals were equally successful in attacking passing fish to feed on dermal tissue/scales, indicating that deceptive strategies used by each colour form may deliver equal fitness benefits. The present study demonstrates for the first time how fangblennies change colour and highlights that colour plasticity offers important adaptive advantage; however, physiological constraints should also be considered

An Ishihara-style test of animal colour vision

ABSTRACT Colour vision mediates ecologically relevant tasks for many animals, such as mate choice, foraging and predator avoidance. However, our understanding of animal colour perception is largely derived from human psychophysics, and behavioural tests of non-human animals are required to understand how colour signals are perceived. Here, we introduce a novel test of colour vision in animals inspired by the Ishihara colour charts, which are widely used to identify human colour deficiencies. In our method, distractor dots have a fixed chromaticity (hue and saturation) but vary in luminance. Animals can be trained to find single target dots that differ from distractor dots in chromaticity. We provide MATLAB code for creating these stimuli, which can be modified for use with different animals. We demonstrate the success of this method with triggerfish, Rhinecanthus aculeatus, which quickly learnt to select target dots that differed from distractor dots, and highlight behavioural parameters that can be measured, including success of finding the target dot, time to detection and error rate. We calculated discrimination thresholds by testing whether target colours that were of increasing colour distances (ΔS) from distractor dots could be detected, and calculated discrimination thresholds in different directions of colour space. At least for some colours, thresholds indicated better discrimination than expected from the receptor noise limited (RNL) model assuming 5% Weber fraction for the long-wavelength cone. This methodology could be used with other animals to address questions such as luminance thresholds, sensory bias, effects of sensory noise, colour categorization and saliency

Chemoecological studies on marine natural products: terpene chemistry from marine mollusks

Some species of nudibranchs (Mollusca) protect themselves from predatory attacks by storing defensive terpene chemicals acquired from dietary sponges (Porifera) in specialized body parts called MDFs (mantle dermal formations), often advertising their unpalatability to potential predators by means of bright coloration patterns. Consequently, the survival of these trophic specialist species is closely related to the possibility of obtaining the defensive tools from sponges that live in their immediate vicinity; therefore, it is important to determine as precisely as possible the chemical composition of nudibranch extracts prior to any ecological studies addressing issues that involve their alimentary behavior and their defensive strategies, including the significance of their color patterns. Some of our recent studies on the chemical composition of terpene extracts from nudibranchs belonging to the genera Chromodoris and Hypselodoris are summarized. We also report the development of a method to assay extracts and purified metabolites for their feeding deterrent activity against co-occurring generalist predators. In a recent chemoecological study, showing that repugnant terpene chemicals are accumulated at extremely high concentrations in exposed parts of the nudibranchs' bodies, the feeding deterrence assays were carried out on the generalist marine shrimp Palaemon elegans, very common in the Mediterranean. We have modified this assay for use with the Australian shrimp species P. serenus, and confirmed the ecological validity of the assay by analysis of extracts from species of sponges and mollusks that live in the same habitat as P. serenus. The deterrent properties of haliclonacyclamine alkaloids isolated from the sponge Haliclona sp. were demonstrated, with the alkaloid mixture demonstrating palatability deterrence at concentrations as low as 0.05 mg/mL, and complete deterrence at 0.75 mg/mL. In contrast, the diterpene thuridillin metabolites from the sacoglossan mollusk Thuridilla splendens did not deter feeding by P. serenus

Colour discrimination thresholds vary throughout colour space in a reef fish (Rhinecanthus aculeatus)

Animals use colour vision in a range of behaviours. Visual performance is limited by thresholds, which are set by noise in photoreceptors and subsequent neural processing. The receptor noise limited (RNL) model of colour discrimination is widely used for modelling colour vision and accounts well for experimental data from many species. In one of the most comprehensive tests yet of colour discrimination in a non-human species, we used Ishihara-style stimulus patterns to examine thresholds for 21 directions at five locations in colour space for the fish Rhinecanthus aculeatus. Thresholds matched RNL model predictions most closely for stimuli near the achromatic point, but exceeded predictions (indicating a decline in sensitivity) with distance from this point. Thresholds were also usually higher for saturation than for hue differences. These changes in colour threshold with colour space location and direction may give insight into photoreceptor non-linearities and postreceptoral mechanisms of colour vision in fish. Our results highlight the need for a cautious interpretation of the RNL model – especially for modelling colours that differ from one another in saturation (rather than hue), and for highly saturated colours distant from the achromatic point in colour space

Toxicity and taste:unequal chemical defences in a mimicry ring

Mimicry of warning signals is common, and can be mutualistic when mimetic species harbour equal levels of defence (Müllerian), or parasitic when mimics are undefended but still gain protection from their resemblance to the model (Batesian). However, whether chemically defended mimics should be similar in terms of toxicity (i.e. causing damage to the consumer) and/or unpalatability (i.e. distasteful to consumer) is unclear and in many studies remains undifferentiated. In this study, we investigated the evolution of visual signals and chemical defences in a putative mimicry ring of nudibranch molluscs. First, we demonstrated that the appearance of a group of red spotted nudibranchs molluscs was similar from the perspective of potential fish predators using visual modelling and pattern analysis. Second, using phylogenetic reconstruction, we demonstrated that this colour pattern has evolved multiple times in distantly related individuals. Third, we showed that these nudibranchs contained different chemical profiles used for defensive purposes. Finally, we demonstrated that although levels of distastefulness towards Palaemon shrimp remained relatively constant between species, toxicity levels towards brine shrimp varied significantly. We highlight the need to disentangle toxicity and taste when considering chemical defences in aposematic and mimetic species, and discuss the implications for aposematic and mimicry signal evolution

Long-Term Effects of the Cleaner Fish Labroides dimidiatus on Coral Reef Fish Communities

Cleaning behaviour is deemed a mutualism, however the benefit of cleaning interactions to client individuals is unknown. Furthermore, mechanisms that may shift fish community structure in the presence of cleaning organisms are unclear. Here we show that on patch reefs (61–285 m2) which had all cleaner wrasse Labroides dimidiatus (Labridae) experimentally removed (1–5 adults reef−1) and which were then maintained cleaner-fish free over 8.5 years, individuals of two site-attached (resident) client damselfishes (Pomacentridae) were smaller compared to those on control reefs. Furthermore, resident fishes were 37% less abundant and 23% less species rich per reef, compared to control reefs. Such changes in site-attached fish may reflect lower fish growth rates and/or survivorship. Additionally, juveniles of visitors (fish likely to move between reefs) were 65% less abundant on removal reefs suggesting cleaners may also affect recruitment. This may, in part, explain the 23% lower abundance and 33% lower species richness of visitor fishes, and 66% lower abundance of visitor herbivores (Acanthuridae) on removal reefs that we also observed. This is the first study to demonstrate a benefit of cleaning behaviour to client individuals, in the form of increased size, and to elucidate potential mechanisms leading to community-wide effects on the fish population. Many of the fish groups affected may also indirectly affect other reef organisms, thus further impacting the reef community. The large-scale effect of the presence of the relatively small and uncommon fish, Labroides dimidiadus, on other fishes is unparalleled on coral reefs

The Evolution of Fangs, Venom, and Mimicry Systems in Blenny Fishes

Venom systems have evolved on multiple occasions across the animal kingdom, and they can act as key adaptations to protect animals from predators. Consequently, venomous animals serve as models for a rich source of mimicry types, as non-venomous species benefit from reductions in predation risk by mimicking the coloration, body shape, and/or movement of toxic counterparts. The frequent evolution of such deceitful imitations provides notable examples of phenotypic convergence and are often invoked as classic exemplars of evolution by natural selection. Here, we investigate the evolution of fangs, venom, and mimetic relationships in reef fishes from the tribe Nemophini (fangblennies). Comparative morphological analyses reveal that enlarged canine teeth (fangs) originated at the base of the Nemophini radiation and have enabled a micropredatory feeding strategy in non-venomous Plagiotremus spp. Subsequently, the evolution of deep anterior grooves and their coupling to venom secretory tissue provide Meiacanthus spp. with toxic venom that they effectively employ for defense. We find that fangblenny venom contains a number of toxic components that have been independently recruited into other animal venoms, some of which cause toxicity via interactions with opioid receptors, and result in a multifunctional biochemical phenotype that exerts potent hypotensive effects. The evolution of fangblenny venom has seemingly led to phenotypic convergence via the formation of a diverse array of mimetic relationships that provide protective (Batesian mimicry) and predatory (aggressive mimicry) benefits to other fishes. Our results further our understanding of how novel morphological and biochemical adaptations stimulate ecological interactions in the natural world